Contrasting effects of Rhizophagus irregularis versus bacterial and fungal seed endophytes on Trifolium repens plant-soil feedback

Interactions between plants and soil affect plant–plant interactions and community composition by modifying soils conditions in plant-soil feedback, where associated microbes have the most crucial role. Both arbuscular mycorrhizal fungi (AMF) and microbial seed endophytes have been demonstrated to influence, directly or indirectly, biotic or abiotic soil properties, thus affecting subsequent plant growth, and community structure. However, little is known about how plant endophyte communities, individually or in interaction with AMF, affect plant-soil feedback processes. Here, we investigated, through a manipulative experiment, the behavior of endophyte-free and endophyte-associated Trifolium repens plants grown in soils previously conditioned by conspecific endophyte-free and endophyte-associated plants, inoculated or not by Rhizophagus intraradices. Furthermore, we identified microbial endophytes directly from the inner tissues of seeds by high-throughput sequencing, to compare seed fungal and bacterial endophyte composition. Results demonstrated that the outcome of simultaneous occurrence of seed endophytes and AMF on plant behavior depended on matching the endophytic status, i.e., either the presence or absence of seed microbial endophytes, of the conditioning and response phase. Seed fungal endophytes generated strong conspecific negative feedback, while seed bacterial endophytes proved to shift the feedback from negative to positive. Moreover, the simultaneous occurrence of both seed endophytes with AMF could either generate or expand negative plant-soil feedback effects. Our results show that seed and root symbionts can play a significant role on setting conspecific plant-soil feedback.